Rearranging development makes a slippery slope: a commentary on ‘Carnivorous Nepenthes pitcher plants combine common developmental processes to make a complex epidermal trapping surface’

Plants interact with their surroundings via the surface of their epidermal cells. For example, many leaves have highly waterproof cuticles, some possess spiky surfaces for defence against herbivores, trees are often covered in thick bark for protection against fire, and many carnivorous plants have very slippery surfaces to ingeniously cause insects to slip into their pitcher traps. Although the diverse utility of plant surfaces is beyond doubt, how plants build them is poorly understood. The study by Lessware et al. (2024) in this issue of Annals of Botany addresses this question by investigating the cellular basis of development of the Nepenthes peristome.

Nepenthes is a diverse genus of over 140 carnivorous plant species that all trap their prey using pitcher traps. Pitcher traps are hollow, highly modified leaves that catch insects by encouraging them to slip and fall inside. To better capture prey, traps of many Nepenthes species possess a particularly fascinating example of a slippery surface. Around the rim of the pitcher is a lip, known as the peristome. The peristome has an intricately patterned surface that is safe for insects to walk on when dry, but becomes very slippery when wet, causing ants and other walking insects to slip and fall into the trap (Bauer et al., 2008). The peristome is also covered in overhanging ridges that allow an insect to move into, but not out of, the trap (Bohn and Federle, 2004). How this highly wettable, directionally slippery surface is built through development was unknown until now.

To understand how the peristome is patterned, Lessware et al. (2024) used scanning electron microscopy to visualize the peristome surface throughout trap development. Although these are static snapshots, the combination of sequential developmental stages allows the authors to infer cell division patterns throughout peristome development. They show that peristome cells undergo three distinct phases of division. Early on in peristome development (at the proto-peristome stage), cells are isodiametric and roughly hexagonal in shape (Fig. 1A). This suggests that cell divisions are roughly equally distributed in all orientations. As the trap grows and differentiates (through the bud differentiation stage), the cells become rectangular in shape and form rows aligned radially around the peristome, suggesting that cells are probably growing anisotropically in the radial orientation and dividing perpendicular to this plane (Fig. 1B). This is followed by a striking change in cell geometry where peristome cells actually decrease in size, maintaining their width but halving in length (Fig. 1C). The fact that this reduction in cell size happens during a period of rapid trap expansion suggests that rapid anisotropic growth and high rates of perpendicular cell division are coordinated. Once this field of roughly square cells has been produced, the cells each produce a single finger-like outgrowth, pointing towards the trap entrance (Fig. 1D). These finger-like projections ultimately overlap and fuse to produce the overhanging ridges that prevent insects from gaining a grip and escaping from the trap.

Fig. 1.

Cell division, expansion and differentiation throughout Nepenthes peristome development. Cells initially maintain a constant size through balanced division and expansion (A and B), then divide in a concerted manner to produce a field of smaller cells (C). These cells then differentiate to produce the patterned peristome surface (D). Scale bars = 200 μm.

During the development of determinate organs (like leaves and most carnivorous traps) plant cells generally undergo proliferation, where cells increase in number and maintain their size, followed by expansion and differentiation where they increase in size and attain their final shape (Fox et al., 2018). In this context, peristome patterning in Nepenthes is highly unusual. The sequence of cellular proliferation–expansion–differentiation is disrupted by a phase of rapid, highly oriented divisions that reduce cell size and produce a field of small cells of equal size. Cell size reduction is not unknown in plant development. Indeed, it is used when producing specialized cell types, such as stomata, through asymmetric divisions (Torii, 2021). However, to my knowledge, no plant tissue has previously been described to undergo a concerted wave of division to globally reduce cell size. Therefore, peristome development seems to rearrange the ‘normal’ sequence of plant development. This highlights the value of investigating development in plants that are not traditional model systems and raises the idea that perhaps to make organs with unusual properties takes some unusual rearranging of development.

The clear outline of peristome development presented in Lessware et al. (2024) raises many questions:

First, what is the role of the temporary increase in division without expansion in peristome patterning? Does it help to make the right cell shape and density to pattern the surface structure of the peristome at the appropriate scale? It will be fascinating to see if Nepenthes species with different surface properties lack this rapid stage of coordinated division, and whether other carnivorous traps or flowers with similarly structured slippery surfaces (Poppinga et al., 2010) also undergo a stage of coordinated cell size reduction.

Although it is not currently possible to transform Nepenthes or other plants that form pitcher traps, in the future it may be possible to perturb gene function using CRISPR or virus-induced gene silencing (VIGS) to test if manipulating cell division patterns perturb peristome slipperiness. This would provide a functional link between cell division and surface properties for the first time and contribute to a more direct engineering of plant surface structure.

Ultimately, the surface properties of any plant structure are due to a combination of its physical shape (formed by cell division and differentiation) and the biochemical properties of the cell wall and cuticle. The developmental progression that Lesware et al. identify provides a clear framework for future work to investigate how cellular and biochemical changes are coordinated through development to pattern the peristome surface. In particular, advances in single cell and spatial transcriptomics (e.g. Nobori et al., 2023) can be applied to key developmental stages of the Nepenthes peristome and begin to identify genes whose expression is altered at particular timepoints, be that during coordinated cell division to reduce cell size, cell shape change during ridge formation or the acquisition of hydrophilic, highly wettable, epidermal cell walls during differentiation. These differentially expressed genes would be strong candidate regulators of peristome development. Work like this will begin to identify molecular mechanisms that sculpt the unusual surface properties of the Nepenthes peristome.

Overall, the study by Lessware et al. (2024) highlights that as plants grow, their cells can not only get bigger, but also smaller, depending on their ultimate cell identity and function. This seemingly strange idea also shows that plants can combine common developmental processes in different ways to make a huge diversity of different structures. It remains to be seen whether the huge suite of genes and hormones that are known to regulate epidermal cell patterning in model plants are also simply rewired to produce novel structures such as the Nepenthes peristome, or whether new gene functions evolved to mediate this developmental rearrangement. Whatever the outcome, the study by Lessware et al. (2024) gives us a first glimpse into the complex development of a highly specialized plant surface, and opens up a variety of interesting questions for study.